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Absorption of N-Phenylpropenoyl-L-Amino Acids in Healthy Humans by Oral Administration of Cocoa (Theobroma Cacao)

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Absorption of N-Phenylpropenoyl-L-Amino Acids in Healthy Humans by Oral Administration of Cocoa (Theobroma Cacao) Mol. Nutr. Food Res. 2008, 52, 1201 – 1214 DOI 10.1002/mnfr.200700447 1201 Research Article Absorption of N-phenylpropenoyl-L-amino acids in healthy humans by oral administration of cocoa (Theobroma cacao) Timo Stark1, Roman Lang1, Daniela Keller1, Andreas Hensel2 and Thomas Hofmann1 1Lehrstuhl fr Lebensmittelchemie und Molekulare Sensorik, Technische Universitt Mnchen, Freising, Germany 2Institut fr Pharmazeutische Biologie und Phytochemie, Mnster, Germany Besides flavan-3-ols, a family of N-phenylpropenoyl-L-amino acids (NPAs) has been recently identi- fied as polyphenol/amino acid conjugates in the seeds of Theobroma cacao as well as in a variety of herbal drugs. Stimulated by reports on their biological activity, the purpose of this study was to inves- tigate if these amides are absorbed by healthy volunteers after administration of a cocoa drink. For the first time, 12 NPAs were quantified in human urine by means of a stable isotope dilution analysis with LC-MS/MS (MRM) detection. A maximum amount was found in the urine taken 2 h after the cocoa consumption. The highest absolute amount of NPAs excreted with the urine was found for N- [49-hydroxy-(E)-cinnamoyl]-L-aspartic acid (5), but the highest recovery rate (57.3 and 22.8%), that means the percentage amount of ingested amides excreted with the urine, were determined for N-[49- hydroxy-(E)-cinnamoyl]-L-glutamic acid (6) and N-[49-hydroxy-39-methoxy-(E)-cinnamoyl]-L-tyro- sine (13). In order to gain first insights into the NPA metabolism in vivo, urine samples were analyzed by LC-MS/MS before and after b-glucuronidase/sulfatase treatment. As independent of the enzyme treatment the same NPA amounts were found in urine, there is strong evidence that these amides are metabolized neither via their O-glucuronides nor their O-sulfates. In order to screen for caffeic acid O-glucuronides as potential NPA metabolites, urine samples were screened by means of LC-MS/MS for caffeic acid 3-O-b-D-glucuronide and 4-O-b-D-glucuronide. But not even trace amounts of one of these glucuronides were detectable, thus excluding them as major NPA metabolites and underlining the importance of future investigations on a potential O-methylation or reduction of the N-phenylpro- penoyl moiety in NPAs. Keywords: Cocoa / (E)-caffeoyl-3-O-b-D-glucuronide / (E)-caffeoyl-4-O-b-D-glucuronide / N-phenylpropenoyl-L- amino acids / Polyphenols / Received: October 28, 2007; revised: December 30, 2007; accepted: January 13, 2008 1 Introduction nol intake and the risk of cardiovascular disease, indicating various potential flavanol-mediated bioactivities, including Epidemiological and medical anthropological investiga- the improvement of vasodilation [1–3], blood pressure [4], tions suggest that flavanol-rich foods exert cardiovascular insulin resistance, and glucose tolerance [5], the attenuation health benefits. Recent dietary interventions in humans of platelet reactivity [6], as well as the improvement of using polyphenol-containing foods have substantiated epi- immune responses and antioxidant defense systems [7, 8]. demiological data on an inverse relationship between flava- The seeds of Theobroma cacao are an important source of polyphenols comprising 12–18% of its total weight on dry Correspondence: Professor Thomas Hofmann, Lehrstuhl fr Leben- basis. Among the cocoa polyphenols, epicatechin smittelchemie und Molekulare Sensorik, Technische Universitt Mn- (249.4 mg/100 g), and procyanidins such as procyanidin B2 chen, Lise-Meitner-Straße 34, D-85354 Freising, Germany (121.4 mg/100 g), procyanidin C1 (138.6 mg/100 g), and E-mail: [email protected] procyanidin B5 (46.4 mg/100 g) were found as the quantita- Fax: +49-8161-71-2949 tively predominating flavan-3-ols in cocoa nibs used as the Abbreviations: HMBC, heteronuclear multiple bond correlation spec- key ingredient for the manufacturing of chocolate and choc- troscopy; HMQC, heteronuclear multiple-quantum correlation spec- olate confectionary [9]. Besides these flavanoids, a family of troscopy; MRM, multiple reaction monitoring; NPAs, N-phenylprope- N-phenylpropenoyl-L-amino acids 1–10 (Fig. 1) has been noyl-L-amino acids; SIDA, stable isotope dilution assay i 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.mnf-journal.com 1202 T. Stark et al. Mol. Nutr. Food Res. 2008, 52, 1201 – 1214 recently identified as polyphenol/amino acid conjugates in (–)-N-[39,49-dihydroxy-(E)-cinnamoyl]-3-hydroxy-L-tyro- cocoa [10, 11]. Among these compounds, N-[39,49-dihy- sine (3, 28.7 mg/100 g), and N-[49-hydroxy-(E)-cinnamoyl]- droxy-(E)-cinnamoyl]-L-aspartic acid (1, 47.2 mg/100 g) L-aspartic acid (5, 13.9 mg/100 g) were found as predomi- Figure 1. Chemical structures of N-phenylpropenoyl-L-amino acids 1–13 and their deuterium-labeled isotopologues d3-1 –d4-13. i 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.mnf-journal.com Mol. Nutr. Food Res. 2008, 52, 1201 – 1214 1203 nating polyphenolic amides in cocoa nibs [9, 12]. Further- chloride, silica gel (70–230 mesh), and formic acid 2 more, amide 3 was identified in red clover (Trifolium pra- (Merck, Darmstadt, Germany). [2,3,5,6- H4]-L-tyrosine tense) [13–15], and together with (–)-N-[49-hydroxy-(E)- was purchased from Cambridge Isotope Laboratories (MA, cinnamoyl]-L-tyrosine (8) was reported as an antioxidant in USA). The enzyme solution containing b-glucuronidase cocoa [16] and as a constituent of the bark of African black- (l100 unit/lL) and sulfatase (l7 unit/lL) from Helix wood (Dalbergia melanoxylon) [17]. In addition (–)-N- pomatia Type HP-2 was purchased from Sigma–Aldrich. [39,49-dihydroxy-(E)-cinnamoyl]-L-tyrosine (4) has been One unit of b-glucuronidase liberated 1.0 lg of phenolph- previously identified in cocoa flowers [18] and together with thalein from phenolphthalein O-glucuronide per hour at the tryptophane derivatives 11 [19] and 12 [20], as well as the pH 5.0 and 378C, one unit of sulfatase hydrolyzed 1.0 lmol tyrosine conjugate 13 were detected in raw robusta coffee of p-nitrocatechol O-sulfate per hour at pH 5.0 and 378C. beans [21]. Very recently, a comprehensive LC-MS/MS Water for chromatographic separations was purified with a screening enabled the identification of several amides in a Milli-Q Gradient A10 system (Millipore, Schwalbach, Ger- variety of herbal drugs; for example, compounds 1, 5, 6, 9, many), and solvents used were of HPLC grade (Merck). and 10 were found in fruits of Coriandrum sativum and flow- Deuterated solvents were obtained from Euriso-Top (Gif- ers of Sambucus nigra as well as Lavandula species, and Sur-Yvette, France). Table water (Evian) from a local sup- compounds 5 and 10 in roots of Angelica archangelica and plier was used for the preparation of the cocoa drink. Alkal- fruits of Phytostigma venenosum [22]. ized cocoa powder prepared from cocoa from Ghana (West Besides their astringent taste activity [9–11] as well as Africa) was obtained from the food industry. their antioxidant properties [16], some of these N-phenyl- propenoyl-L-amino acids were found to be biologically 2.2 Preparation of the cocoa drink and analysis of active as phytoallexins [23], as inducers of mitochondrial N-phenylpropenoyl-L-amino acids activity and proliferation rate in human liver cell lines as well as human keratinocytes [22], and as potent inhibitor of A mixture of alkalized cocoa powder (20.3 g) and sucrose the adhesion of Helicobacter pylori to human stomach tis- (3.0 g) was suspended in table water (400 mL) at 508C for sue [22]. In consequence, there is a growing interest in the 10 min whilst stirring. After cooling, this cocoa drink was human bioavailability of these nitrogen-containing phyto- used for the human intervention study as well as for chemi- chemicals from foods. Although it is generally believed that cal analysis. the bioavailability of intact polyphenols including hydroxy- For quantitative determination of N-phenylpropenoyl-L- cinnamic acid esters is rather poor [24], there are no data amino acids by means of a recently developed stable isotope available on the human bioavailability of N-phenylprope- dilution analysis [12], an aliquot of the cocoa drink noyl-L-amino acids consisting of a hydroxycinnamic acid (105.0 g) was spiked with solutions (100 lL, each) of the linked to an amino acid via an amide bond. labeled internal standards d3-1, d3-3, d4-4, d3-5, d3-7, d4-8, The objective of the present study was, therefore, to d3-10, d5-11, d5-12, and d4-13 in methanol (1.0 mg/mL) and administer a cocoa drink containing defined amounts of N- the mixture was homogenized and equilibrated for 30 min phenylpropenoyl-L-amino acids to healthy volunteers and whilst moving in a lab shaker. Thereafter, the cocoa drink to quantitatively follow the urinary excretion of these was freeze-dried, the powder was extracted with n-pentane amides over time. As the use of stable isotopologues of ana- (5630 mL) for 30 min, and the residual cocoa material was lytes is known to enable the correction of compound dis- extracted five times with acetone/water (70:30 v/v; 30 mL criminating during extraction, cleanup, chromatographic each) for 45 min at room temperature whilst stirring. After separation, as well as MS detection, the recently developed centrifugation, the liquid layer was freed from acetone stable isotope dilution assay (SIDA) with LC-MS/MS mul- under reduced pressure at 308C, and then freeze-dried to tiple reaction monitoring (MRM) detection [12] was used give the acetone/water extract. Aliquots (about 40 mg) of as a versatile and reliable method to ensure the accurate the acetone/water extract were taken up in methanol/water quantification of these phytochemicals. (1:1 v/v; 10 mL) and adjusted to pH 2.5 with formic acid.
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